January 24, 2012

The Evolution and Neuromechanics of very-fast movements

How are movements completed in under a millisecond (ms) generated and regulated, particularly when they result in forces many times the body weight of the organism in question? Much of the recent work (over the last 15-20 years) has focused on neuromuscular, sensory, and mechanical mechanisms. Some people have proposed a field called neuromechanics [1, 2] to synthesize how animals process sensory information and use it for adaptive movement. A neuromechanical approach requires a feedback loop between sensory stimuli and muscular output, mediated by neural mechanisms. One simple example of this is control of the gill structure in Sea Slugs (Aplysia). Using a series of conditioned stimuli, the gill structure will open and close in an adaptive manner similar to the learning and memory found in more complex neural systems.

On the January 20th episode of Science Friday (an NPR show on Friday afternoons), the video clip of the week featured work from the Patek Lab at UMass-Amherst. The Patek Lab focuses on the very fast predatory and fighting movements seen in Mantis Shrimp (Stomatopods) and Trap Jaw Ants (Odontomachus). By looking into the work being done at the Patek Lab, I was introduced to an entire body of work on ultra-fast and very powerful movements. This work is very cutting-edge, and provides a wealth of information on evolution, behavior, and the function of neuromuscular systems.

How does a mechanism specialized for rapid and powerful movements evolve and vary across phylogeny? In a paper by Spagna et.al [3], a phylogeny of trap-jaw ants was constructed by using observations of behaviors related to appendage usage, mechanical function, and several genetic loci. The authors were trying to trying to correlate differences in the speed and acceleration of appendage movement with morphological variation as observed across all species in the genus (see Figure 1).These findings suggest a recent origin and rapid diversification for appendage mechanisms.

Figure 1: Phylogenetic relationships between species of trap-jaw ant. Taken from [3].

Why do trap-jaw ants need to produce large amounts of force relative to their body weight, and why is it variable across evolution? While using their mandibular appendage, trap jaw ants produce a stress (force) that is 300x their own body weight [4]. This produces a movement so fast that it could not be studied until the proper high-speed motion capture equipment became available. If the ants strike the ground with their appendage, they can produce a movement called “ballistic” jumping, which results in an uncontrollable jump.

The authors of [4] refer to mandibular appendage closure as a "high-performance" behavior. In general, high-performance behaviors are associated with a single function. However, appendage closure is a multifunctional behavior, used for prey capture, fighting, and jumping to safety [4]. Perhaps more interestingly, multifunctional behaviors are related to evolutionary tradeoffs and the co-option (or exaptation) of shared and novel structures. In [3], it is suggested that size might be limited by energetic constraints but maximized by the requirements of prey capture. Yet since the production of force is many times larger than the organism produces in any other muscle, there could be other dynamics at work here, including evolutionary arms races within species.

In Figure 2, we can see the location of the mandibular appendage in relation to the anterior portion of their body. When this appendage strikes the ground, it produces the ballistic movement also seen in Figure 2. Ballistic movements are essentially bursts of muscular activity produced without much regard for control. Throwing, kicking, and eyeball saccade movements are examples of ballistic movements in humans.

Figure 2. LEFT: image of mandibular appendange. RIGHT: frames from video of a jaw propulsion movement. Taken from [3].

In the study of human movement, there is a notion called the speed-accuracy tradeoff, characterized by Fitts’ Law [5]. In essence, the faster the movement, the less accurate it will be. This has much to do with the lack of muscular control for movements that generate a large amount of force in a short period of time [6]. Highly-controlled movements such as drawing or balancing require that movements be made slowly and no large fluctuations in force be introduced. This requires extensive co-regulation of muscle groups, and results in a highly complex sequence of physiological events. Very fast movements, on the other hand, are produced simply by letting a single muscle or muscle group release the maximum amount of force that it is capable of producing.

Now that we know how muscle force production can be maximized with respect to output, we must now understand how muscle power is “amplified” in nature. From the standpoint of technology, we know how to amplify the amount of work done by a set of muscles in the human body. But how is this accomplished naturally? One way is via kinematic or mechanical linkage. In the human body, a whole-body movement such as a heave involves movement of the trunk, arms, and fingers. As one moves outward from the midline, the velocity and acceleration of a segment (e.g. humerus, forearm, or hand) become progressively larger and less uniform with regard to time. Now consider how the mantis shrimp uses its appendage. Unlike the trap jaw ant mandibular appendage, the mantis shrimp appendage is used for cracking open the shells of prey. This requires massive forces to be produced and displaced, but which also requires a highly specialized phenotype.

Muscle power amplification in the mantis shrimp works in a similar manner. Muscle power can be thought of as the amount of potential work done by the muscle [7]. Muscle “work” is related to the amount of force generated by the muscle and the appendage it is connected to. In [8] and [9], it is suggested that extremely fast movements for which power amplification is required are achieved by reducing the duration of the movement. The anatomical linkage involved in power amplification is the integrated function of three units (Figures 3 and 4): an engine, an amplifier, and a tool [9]. In the context of mantis shrimp anatomy, the engine is represented by muscle, while the amplifier is represented by spring and the tool is represented by a hammer. Consistent with the notion of kinematic linkage, the distal component of this system produce the greatest forces (and of course move the fastest).

Figure 4. LEFT: cartoon of the mantis shrimp appendage and a geometric model that approximates shape changes in anatomical structure. RIGHT: images of the mantis shrimp during behavior and after dissection/maceration. Taken from [8].

In [9], the authors consider the developmental origins of the muscle power amplifier system. To do this, they ask two questions. The first is whether or not the three components of the appendage system (muscle, merus region, and hammer) constitute three independent developmental modules. Since this is found to be the case, the second question centers around the scaling of the appendage system with respect to body size. The answer to this is yes, but with some interesting qualifications. As expected, muscle force increases proportionally to muscle shape and size. Yet there is a lack of change in shape relative to size, which is different from the isometric relationship between muscle size and body mass seen in jumping and running mammals. In addition, the merus region (the “spring” mechanism) has a selective capacity for stiffness, which results in maximal force production that scales allometrically to body size. Finally, the hammer (the “tool” mechanism) acts as a lever, which like the human foot provides a mechanical advantage to handling large loadings and forces.